Time course and reversibility of changes in the gizzards of red knots alternately eating hard and soft food.

The ability to change organ size reversibly can be advantageous to birds that perform long migrations. During winter, red knots (Calidris canutus) feed on shellfish and carry a muscular gizzard that weighs 10% of their body mass. Gizzard size decreases when these birds eat soft foods, e.g. while breeding in the tundra. We studied the reversibility and time course of such changes using ultrasonography. Two groups of shellfish-adapted knots (N=9 and N=10) were fed alternately a hard and a soft food type. Diet switches elicited rapid reversible changes. Switches from hard to soft food induced decreases to 60% of initial gizzard mass within 8.5 days, while switches to hard food induced increases in gizzard mass to 147% within 6.2 days. A third group of knots (N=11), adapted to soft food for more than 1 year, initially had very small gizzards (25% of the mass of shellfish-adapted gizzards), but showed a similar capacity to increase gizzard size when fed shellfish. This is the first non-invasive study showing rapid digestive organ adjustments in non-domesticated birds.

Is long-distance bird flight equivalent to a high-energy fast? Body composition changes in freely migrating and captive fasting great knots.

We studied changes in body composition in great knots, Calidris tenuirostris, before and after a migratory flight of 5,400 km from northwest Australia to eastern China. We also took premigratory birds into captivity and fasted them down to their equivalent arrival mass after migration to compare organ changes and nutrient use in a low-energy-turnover fast with a high-energy-turnover fast (migratory flight). Migrated birds were as economical as any fasting animal measured yet at conserving protein: their estimated relative protein contribution (RPC) to the energy used was 4.0%. Fasted birds had an estimated RPC of 6.8% and, consequently, a much lower lean mass and higher fat content for an equivalent body mass than migrated birds. Lean tissue was catabolized from most organs in both groups, except the brain. Furthermore, a principal components biplot showed that individuals were grouped primarily on the basis of overall organ fat or lean tissue content rather than by the size of specific organs. This indicates that organ changes during migratory flight are similar to those of a low-energy fast, although the length of the fast in this study probably accentuated organ reductions in some functional groups. Whether the metabolic characteristics of a flying migratory fast follow the three-phase model described in many inactive fasting animals is unclear. We have some evidence for skeletal fat being catabolized without phase 3 of a fast having been reached.

Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling.

We used ultrasonic imaging to monitor short-term changes in the pectoral muscle size of captive red knots Calidris canutus. Pectoral muscle thickness changed rapidly and consistently in parallel with body mass changes caused by flight, fasting and fuelling. Four knots flew repeatedly for 10 h periods in a wind tunnel. Over this period, pectoral muscle thickness decreased in parallel with the decrease in body mass. The change in pectoral muscle thickness during flight was indistinguishable from that during periods of natural and experimental fasting and fuelling. The body-mass-related variation in pectoral muscle thickness between and within individuals was not related to the amount of flight, indicating that changes in avian muscle do not require power-training as in mammals. Our study suggests that it is possible for birds to consume and replace their flight muscles on a time scale short enough to allow these muscles to be used as part of the energy supply for migratory flight. The adaptive significance of the changes in pectoral muscle mass cannot be explained by reproductive needs since our knots were in the early winter phase of their annual cycle. Instead, pectoral muscle mass changes may reflect (i) the breakdown of protein during heavy exercise and its subsequent restoration, (ii) the regulation of flight capacity to maintain optimal flight performance when body mass varies, or (iii) the need for a particular protein:fat ratio in winter survival stores.

Empirical evidence for differential organ reductions during trans-oceanic bird flight.

Since the early 1960s it has been held that migrating birds deposit and use only fat as fuel during migratory flight, with the non-fat portion of the body remaining homeostatic. Recent evidence from field studies has shown large changes in organ sizes in fuelling birds, and theory on fuel use suggests protein may be a necessary fuel during flight. However, an absence of information on the body condition of migrants before and after a long flight has hampered understanding of the dynamics of organs during sustained flight. We studied body condition in a medium-sized shorebird, the great knot (Calidris tenuirostris), before and after a flight of 5400 km from Australia to China during northward migration. Not only did these birds show the expected large reduction in fat content after migration, there was also a decrease in lean tissue mass, with significant decreases in seven organs. The reduction in functional components is reflected in a lowering of the basal metabolic rate by 42% [corrected]. Recent flight models have tried to separate the 'flexible' part of the body from the constant portion. Our results suggest that apart from brains and lungs no organs are homeostatic during long-distance flight. Such organ reductions may be a crucial adaptation for long-distance flight in birds.

Estimating organ size in small migrating shorebirds with ultrasonography: An intercalibration exercise.

Organs, even of fully grown adult birds, mammals, and reptiles, may show substantial size changes in relation to specific performances. These changes are difficult to study, because measurements usually can only be obtained following the death of the animal. We explored the use of ultrasonographic imaging, a relatively simple noninvasive technique, to measure size of pectoral muscles and stomach in two small shorebird species (red knots Calidris canutus and golden plovers Pluvialis apricaria). Accuracy of ultrasound measurements in estimating organ mass in red knots was reasonably high. Depending on the equipment used, the error of individual measurements was 20%-25% for the pectoral muscles and 26%-44% for the stomach. In plovers the technique was less accurate, probably because of the low variability of the organs involved. Ultrasound scanning is particularly suited to measure rapidly changing organ sizes over short time intervals. We demonstrate this with an example in which changes in individuals in size of pectoral muscle and stomach were monitored in captive red knots following a change in diet. Ultrasound measures will enable studies on the links between body composition and future behavior and physiology.

Daily energy budgets of avian embryos: the paradox of the plateau phase in egg metabolic rate.

The metabolic rate of precocial bird eggs reaches a plateau when about 80% of the incubation period has passed. This is unexpected, as in many species the embryo continues to grow and maintenance costs must therefore increase. To investigate this paradox, daily energy budgets were constructed for embryos of four galliform species according to two models that used empirical data on egg metabolic rate and embryo growth. In the first model, embryonic synthesis costs were estimated, with an assumed synthesis efficiency, before calculating the maintenance costs. In the second model, embryonic maintenance was calculated first, and no assumptions were made on the synthesis efficiency. The calculations show that assumptions of the synthesis efficiency had a major impact on the energy budget calculations, because embryonic growth rate was high. During the plateau phase, a galliform embryo allocated energy in favor of its maintenance costs in three ways: by decreasing growth rate, by increasing synthesis efficiency, and by depressing the formation of glycogen. Our study suggests that a reduction in growth rate plays a minor role. An increase of synthesis efficiency is more likely to explain the plateau in energy expenditure, since small increases in synthesis efficiency can lead to great savings on synthesis costs.

Growth rate and maturation of skeletal muscles over a size range of galliform birds.

The relationship between growth rate and development of function in leg and pectoral muscles was studied in four species of galliform birds ranging from 125 g to 18 kg and, for comparison, in an altricial species, the European starling (80 g). An index to neonatal maturity (muscle dry content proportion as a fraction of adult value) was higher in leg than in pectoral muscles and lower in larger than in smaller galliforms. The maturity index was substantially lower in starling neonates. After the first week posthatch, however, the maturity index was highest in larger species. Exponential growth rates decreased linearly with increasing maturity in both pectoral and leg muscles, following similar regressions in all species including the starling. At a particular value of the maturity index, the exponential growth rate was higher in pectoral than in leg muscles. The exponential growth rates of muscles of neonatal large galliforms were lower than expected from their low maturity. This may represent the down-regulation shortly after hatching of the high exponential growth rate needed to reach a large hatching mass in a short incubation period. A slower growth rate immediately posthatch may be necessary if the relatively immature neonatal digestive system cannot deliver nutrients or metabolized energy required for more rapid growth. Smaller species may not be faced with the constraint of rapid growth toward the end of the embryonic period.

Effect of growth rate and body mass on resting metabolic rate in galliform chicks.

In this study, we asked whether within-species variation in chick resting metabolic rate was related to variation in growth and whether this relationship changed during development in three galliform species (turkey, Meleagris gallopavo, guinea fowl, Numida meleagris, and Japanese quail, Coturnix coturnix japonica). Resting metabolic rate increased by a bi- or triphasic pattern with body mass. For each phase, the relationship between metabolic rate and growth was studied by residual analysis, with two measures of growth: growth rate and body mass. Chick mass reflects the net result of accumulated growth, while hatchling mass reflects embryonic growth. In hatchlings, high metabolic rates coincided with low growth rates in turkeys and guinea fowl. These species delay initial food intake, and under these circumstances high metabolic expenditure may preclude conversion of yolk energy into body mass. No relationship was present between residual hatching metabolic rate and residual body mass. In older chicks, residual metabolic rate was positively linearly related with residual growth rate (turkeys and young quail) or residual body mass (guinea fowl and older quail). The similarity of the slopes suggests that growth rate and accumulated growth affected maintenance metabolism to the same extent throughout development. These findings suggest that growth models must take ontogenetic adjustments of metabolic rate into account in addition to costs of maintenance.